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Neurocognition in college-aged daily marijuana

users
a a a
Mary P. Becker , Paul F. Collins & Monica Luciana
a
Department of Psychology, Center for Neurobehavioral Development, University of
Minnesota, Minneapolis, MN, USA
Published online: 12 Mar 2014.

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To cite this article: Mary P. Becker, Paul F. Collins & Monica Luciana (2014) Neurocognition in college-
aged daily marijuana users, Journal of Clinical and Experimental Neuropsychology, 36:4, 379-398, DOI:
10.1080/13803395.2014.893996

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 Journal of Clinical and Experimental Neuropsychology, 2014
Vol. 36, No. 4, 379–398, http://dx.doi.org/10.1080/13803395.2014.893996

Neurocognition in college-aged daily marijuana users

Mary P. Becker, Paul F. Collins, and Monica Luciana
Department of Psychology, Center for Neurobehavioral Development, University of Minnesota,
Minneapolis, MN, USA

(Received 3 September 2013; accepted 7 February 2014)

Background: Marijuana is the most commonly used illicit substance in the United States. Use, particularly when it
Downloaded by [Universidad Nacional Colombia] at 12:24 09 February 2015

occurs early, has been associated with cognitive impairments in executive functioning, learning, and memory.
Method: This study comprehensively measured cognitive ability as well as comorbid psychopathology and
substance use history to determine the neurocognitive profile associated with young adult marijuana use.
College-aged marijuana users who initiated use prior to age 17 (n = 35) were compared to demographically
matched controls (n = 35). Results: Marijuana users were high functioning, demonstrating comparable IQs to
controls and relatively better processing speed. Marijuana users demonstrated relative cognitive impairments in
verbal memory, spatial working memory, spatial planning, and motivated decision making. Comorbid use of
alcohol, which was heavier in marijuana users, was unexpectedly found to be associated with better performance
in some of these areas. Conclusions: This study provides additional evidence of neurocognitive impairment in the
context of adolescent and young adult marijuana use. Findings are discussed in relation to marijuana’s effects on
intrinsic motivation and discrete aspects of cognition.

Keywords: Marijuana; Neurocognition; Decision making; Memory; Planning.

Marijuana is the most commonly used illicit drug
in the United States among adolescents and young
adults, with 52.2% of 18–25-year-olds reporting
use during their lifetimes (Substance Abuse and
Mental Health Services Administration, 2013).
Currently, adolescents and young adults perceive
the risks of marijuana use to be lower, and profess
less disapproval of peer marijuana use, than in past
years (Johnston, Bachman, & Schulenberg, 2012;
Johnston, O’Malley, Bachman, & Schulenberg,
2013). Despite these popular perceptions that mar-
ijuana use is not a high-risk activity, a growing
body of research indicates that use is associated
with cognitive impairments. Given growing
advocacy for marijuana’s legalization and its pre-
valence of use, it is crucial to understand better the
nature of these impairments.
The primary psychoactive compound in mari-
juana, delta-9-tetrahydrocannabinol, acts directly
on the central and peripheral nervous systems,
binding to receptors for endogenous cannabinoids.
Dense populations of endocannabinoid system
(ECS) receptors are located in the prefrontal cor-
tex, hippocampus, basal ganglia, thalamus,
hypothalamus, and cerebellum. Within these
regions, the ECS broadly modulates synaptic sig-
naling (Freund, Katona, & Piomelli, 2003;
Viveros, Llorente, Moreno, & Marco, 2005).

Acknowledgements: We thank Snežana Urošević for helpful comments on prior versions of the manuscript. We also thank Brittany
Schmaling for her contribution to data collection.
Funding: This study was supported by the National Institute on Drug Abuse [grant number R01DA017843] awarded to M. Luciana;
the National Institute on Alcohol Abuse and Alcoholism [grant number R01AA020033] awarded to M. Luciana; and the University of
Minnesota’s Center for Neurobehavioral Development. M. P. Becker was supported by the Pearson Assessment Fellowship in Clinical
Psychology awarded by the Pearson Clinical Assessment Division. Disclosure: Role of funding source: Nothing declared. Funding
sources had no involvement in study design; in the collection, analysis and interpretation of data; in the writing of the report; and in the
decision to submit the paper for publication.
Conflict of interest: No conflict declared by any authors.
Address correspondence to: Mary P. Becker, Department of Psychology, University of Minnesota, S344 Elliott Hall, 75 East River
Road, Minneapolis, MN 55455, USA (E-mail: petr0308@umn.edu).

© 2014 Taylor & Francis

 380 BECKER, COLLINS, LUCIANA
Animal models indicate that the endocannabinoid
system undergoes dramatic change during adoles-
cence (Ellgren et al., 2008; Rodriguez de Fonseca,
Ramos, Bonnin, & Fernandez-Ruiz, 1993). ECS
receptor expression is lower in subcortical
(Rodriguez de Fonseca et al., 1993) and frontal
cortical regions (Ellgren et al., 2008; Heng,
Beverley, Steiner, & Tseng, 2011) in adulthood
than during earlier stages of development.
ECS receptors in the dorsolateral prefrontal cor-
tex (DLPFC) are located in the presynaptic term-
inals of inhibitory GABAergic (GABA = gamma-
aminobutyric acid) interneurons (L. E. Long, Lind,
Webster, & Weickert, 2012). ECS receptor activa-
tion results in excitation through inhibition of the
Downloaded by [Universidad Nacional Colombia] at 12:24 09 February 2015
inhibitory GABAergic interneurons. Normative
patterns of modulation of the ECS through adoles-
cence may be a mechanism through which greater
degrees of cognitive control are achieved. That is,
as ECS receptors are pruned as part of the norma-
tive changes in brain structure that occur during
adolescence (Gogtay & Thompson, 2010), greater
neuronal inhibition develops in the DLPFC,
increasing capacities for cognitive control, self-
directed behavior, and other regulatory functions
(L. E. Long et al., 2012).
Disruption of the ECS during adolescence
through the introduction of outside cannabinoids
can have long-term effects on synaptic transmission
and associated behaviors, leading to persistent
alterations in adulthood. In rodents, chronic canna-
binoid administration during adolescence is linked
to decreased adult serotonergic activity in the brain
stem (Bambico, Nguyen, Katz, & Gobbi, 2010) and
blunted dopamine activity in the midbrain (Pistis
et al., 2004). Rodents exposed to exogenous canna-
binoids during adolescence demonstrate decreased
memory and learning ability (Jager & Ramsey,
2008; Rubino et al., 2009; Schneider & Koch,
2003, 2007) as well as decreased inhibitory control
(Realini, Rubino, & Parolaro, 2009; Schneider &
Koch, 2003) in adulthood.
Similarly, cognitive impairments are noted in
human adolescents and young adults in the context
of active marijuana use. As might be expected,
impairments are evident during acute intoxication,
including impaired attention, executive function,
decision-making skills, and memory function
(Crean, Crane, & Mason, 2011; Morrison et al.,
2009; Ramaekers et al., 2006). Beyond acute intox-
ication, adolescent and young adult marijuana use is
associated with numerous impairments, particularly
in verbal memory and executive functioning.
Marijuana users demonstrate poorer retrospective
recall on list-learning tasks (Bolla, Brown, Eldreth,
Tate, & Cadet, 2002; Gonzalez et al., 2012; Hanson
et al., 2010; Harvey, Sellman, Porter, & Frampton,
2007; Solowij et al., 2011; Takagi et al., 2011) as well
as poorer memory for stories (Fried, Watkinson, &
Gray, 2005; Medina et al., 2007; Schwartz,
Gruenewald, Klitzner, & Fedio, 1989). Similarly,
marijuana users display diminished memory for
future actions assessed through prospective memory
tasks (Bartholomew, Holroyd, & Heffernan, 2010;
McHale & Hunt, 2008; Montgomery, Seddon, Fisk,
Murphy, & Jansari, 2012).
Executive functioning skills appear to be dimin-
ished in marijuana users as well. Marijuana users
show decreased planning ability on a Tower of
London task (Grant, Chamberlain, Schreiber, &
Odlaug, 2012) and a task of logical organization
(Montgomery et al., 2012). Marijuana users demon-
strate less flexibility and abstract reasoning ability
than nonusers (Bolla et al., 2002; Pope & Yurgelun-
Todd, 1996), and decision making tends to be more
risky (Clark, Roiser, Robbins, & Sahakian, 2009;
Grant et al., 2012; Solowij et al., 2012).
Marijuana users demonstrate impairments incon-
sistently in other cognitive domains, including atten-
tion (Bolla et al., 2002; Dougherty et al., 2013;
Lisdahl & Price, 2012), processing speed (Fried
et al., 2005; Lisdahl & Price, 2012; Medina et al.,
2007), and spatial reasoning (Harvey et al., 2007;
Pope & Yurgelun-Todd, 1996). It is unclear whether
performance in these domains is directly related to
marijuana use, or whether other behaviors associated
with marijuana use contribute to these findings.
Deficits remain during early (Cuttler,
McLaughlin, & Graf, 2012; Dougherty et al.,
2013; Fried et al., 2005; McHale & Hunt, 2008)
and sustained (Bolla et al., 2002; Hanson et al.,
2010; Lisdahl & Price, 2012; Medina et al., 2007)
abstinence.
As lawmakers grapple with questions about the
legalization of marijuana, studies of nonacutely
intoxicated marijuana users allow us to understand
how cognitive functioning may be affected in the
context of regular marijuana use. In addressing
that question, it is important to consider when
individuals began to use the drug. Marijuana
users who begin use early in life often demonstrate
greater cognitive impairment than later onset mar-
ijuana users on measures of memory and executive
functioning (Ehrenreich et al., 1999; Fontes et al.,
2011; Gruber, Sagar, Dahlgren, Racine, & Lukas,
2012; Lisdahl, Gilbart, Wright, & Shollenbarger,
2013; Pope et al., 2003). Given the important role
of the ECS during development, it is likely that
disruption of the system at a younger age impacts
later cognitive performance, particularly executive
functions that emerge as frontostriatal brain net-
works reach their full maturational potential.
 NEUROCOGNITION IN MARIJUANA USERS 381

Two important difficulties emerge when trying to
compare studies of young adult marijuana users.
First, the age range tends to vary widely between
studies. Studies exploring samples of college-aged
subjects commonly use a broad age and developmen-
tal range, including people in their late twenties or
thirties (Battisti et al., 2010; Bolla et al., 2002;
Ehrenreich et al., 1999; Wagner, Becker, Gouzoulis-
Mayfrank, & Daumann, 2010; Whitlow et al., 2004).
While several studies have focused on adolescent mar-
ijuana users (Hanson et al., 2010; Harvey et al., 2007;
Medina et al., 2007), it is not common to narrowly
define age groups in young adult samples. Second, the
majority of studies exploring neurocognitive profiles
of adolescent marijuana users focus on a limited range
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selective age band has the benefit of providing infor-
mation regarding the functional skills and abilities
of actively and heavy-using individuals who are
otherwise at low risk for impairment.
Users were compared to nonusing controls in the
context of an assessment battery that included
measures of clinical symptoms, other externalizing
behaviors, and neurocognition across multiple
domains of function.
It was predicted that marijuana users would
exhibit relative impairments in learning and mem-
ory, particularly when such skills recruit executive
functions, as well as decision making, working
memory, and planning.

of cognitive skills. This approach fails to provide a

comprehensive cognitive profile, likely resulting in a
limited understanding of any observed cognitive def-
icits. A broad assessment of cognitive ability can
better reveal patterns of weaknesses but also potential
strengths.
The current study provides a comprehensive cog-
nitive profile of non-treatment-seeking college stu-
dent marijuana users in a narrow age range (18–20
years). Participants were heavy marijuana users but
had histories of typical development and were low
risk in relation to socioeconomic vulnerabilities,
comorbid psychopathology, and general cognitive
ability. Marijuana use in 18–20-year-olds is com-
mon, and the assessment of cognition within this
METHOD
Participants
Seventy-three individuals, ages 18–20 years, were
studied: healthy nonusing controls (n = 37) and
heavy marijuana users who began use before age
17 (n = 36). The average age of use onset was 15.2
years (Table 1). Participants were recruited
through university advertisements, and all were
monetarily compensated.
Controls were selected from a larger study
exploring adolescent brain development (described
in more detail in Luciana, Collins, Olson, &

TABLE 1
Demographic and substance use characteristics of marijuana users and controls

Control (n = 35) Marijuana user (n = 35)

Participant characteristics M (SD) % M (SD) Range % F or χ2 U

Age (years) 19.40 (0.93) 19.52 (0.62) 0.39

Sex ratio (male:female) 13:22 22:13 4.63*
Race (% Caucasian) 77.14 88.57 1.61
Years of education 13.26 (1.24)a 13.29 (0.94)a 0.01
Estimated Full Scale IQa 114.73 (9.40) 115.27 (9.56) 0.05
Vocabulary T-scorea 62.10 (6.85) 61.27 (7.88) 0.21
Matrix reasoning T-scorea 54.49 (5.98) 56.09 (5.21) 1.35
Alcohol use average –0.59 (0.69) 0.59 (0.76) 46.54**
ASR substance use
Past 6 months: Tobacco use per day 0.00 (0.00) 0.91 (1.55) 385.00**
Past 6 months: Days drunk 5.37 (9.24) 25.07 (18.38) 142.00**
Past 6 months: Days using drugs 0.14 (0.49) 145.94 (40.58)a 636.00**
Marijuana useb
Age first used (years) 15.24 (1.24)
Past year: Days MJ used 333.43 (43.61) 208–365
Past 30 days: Days MJ used 25.86 (3.24) 20–28
Past year: Avg. hits per day 10.09 (8.82) 2–50
Past 30 days: Avg. hits per day 10.20 (9.12) 1.5–50
Lifetime: Max hits in 24 hours 38.72 (27.52) 6–120

Notes. Mann–Whitney Us were computed when appropriate. ASR = Adult Self-Report; MJ = marijuana; avg. = average.
a
Marginal means presented, controlling for sex. bVariables only included for marijuana users.
*p ≤ .05. **p ≤ .01.
 382 BECKER, COLLINS, LUCIANA
Schissel, 2009; Olson et al., 2009). Controls were
excluded if they met current or past Axis I DSM–
IV–TR (Diagnostic and Statistical Manual of
Mental Disorders–Fourth Edition, Text Revision;
American Psychiatric Association, 2000) criteria
for any psychiatric disorder and/or if they reported
marijuana use more than once monthly.
General inclusion criteria included being a native
English speaker, being right-handed, with normal/
corrected-to-normal vision and hearing, and having
no reported history of neurological problems, men-
tal retardation, or current pregnancy.
Inclusion criteria for marijuana users consisted of
self-reported marijuana use of at least five times per
week for at least 1 year. Use onset was required to be
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before age 17 so that length of use across study
participants would be relatively uniform. Marijuana
use during this age span has been most strongly
associated with cognitive impairment (Lisdahl et al.,
2013), and use initiation is most common between the
ages of 16 and 18 years in the United States
(Substance Abuse and Mental Health Services
Administration, 2013). Marijuana users were
excluded if they were daily cigarette smokers, if alco-
hol use exceeded four drinks for females and five
drinks for males on more than two occasions per
week, or if they met criteria for current or past sub-
stance dependence other than marijuana. One mar-
ijuana user met criteria for current and past alcohol
dependence, despite meeting the project’s use fre-
quency criteria, and was excluded from analyses.
Marijuana users were asked to refrain from drug
use for at least 12 hours before testing so as not to
be acutely high during the assessment. Longer peri-
ods of abstinence were not required, because we did
not wish to study individuals in the midst of drug
withdrawal and because a goal of the study was to
capture functional capacities in the context of active
use. Formal drug testing was not implemented due to
budgetary limitations and given that the study did
not require long-term marijuana abstinence. This
study was approved by the University of
Minnesota’s Institutional Review Board.
Participants provided informed consent prior to
participation.
Procedure
Interested participants (those who responded to
posted advertisements) completed a phone screening
followed by an in-person structured interview, the
Kiddie Schedule for Affective Disorders and
Schizophrenia Present and Lifetime Version (K-
SADS-PL: Kaufman et al., 1997) to assess for recent
and past histories of psychological problems. The
benefit of using the K-SADS to assess psychopathol-
ogy in young adults is that it captures past histories of
childhood disorders while also providing an in-depth
assessment of DSM–IV-based adult psychopathol-
ogy. Current (recent) ratings were based on the pre-
vious 2 months for non-substance-use-related
disorders and the previous 6 months for substance
use disorders (SUDs). In addition, information was
obtained about quantity and frequency of drug use
across the past 30 days and past year. Intelligence was
estimated by the Vocabulary and Matrix Reasoning
subtests of the Wechsler Abbreviated Scale of
Intelligence (WASI: Wechsler, 1999). Participants
completed detailed health and demographic question-
naires. Participants who met inclusion criteria
returned for a second assessment, including beha-
vioral questionnaires and a comprehensive neurocog-
nitive battery. The battery was designed to capture a
broad array of functions in the domains of motor
behavior, processing speed, attention, spatial, and
verbal memory, and executive skills.
Neurocognitive battery
Motor function
Finger Tapping Test (Lezak, Howieson, &
Loring, 2004). This test measures motor speed.
Participants tapped a key as many times as possi-
ble within a 10-s period. Three trials were adminis-
tered for each hand, and the number of taps per
trial was recorded. The average of all three trials
per hand is reported.
Grooved Pegboard (Lafayette Instrument,
1989). This test measures psychomotor dexterity
and speed. Participants were presented with a flat
board containing rows of holes and small metal
“pegs” that fit into the holes on the board. The
pegs were shaped so that one side is square. Each
peg had to be correctly manipulated in order to fit
the holes. Under timed conditions, participants
used the pegs to fill the holes on the board using
first the right hand, then the left hand. Accuracy
and response time were recorded.
Processing speed
Digit Symbol (Wechsler Adult Intelligence
Scale–Third Edition, WAIS–III, Digit Symbol:
Lezak et al., 2004; Wechsler, 1997). This test mea-
sures psychomotor performance, sustained atten-
tion, response speed, and visuomotor
coordination. This test was administered according
to WAIS–III standardized procedures. The score

recorded is the number of squares filled in correctly
out of a total possible 133 squares.
Letter cancellation task (Lezak et al.,
2004). This task measures immediate attention
and vigilance but is also a speeded test.
Participants viewed a piece of paper on which
were printed rows of capitalized letters. They
were instructed to work as quickly but as accu-
rately as possible and to cross out all occurrences
of the letters “E” and “C.” Time-to-completion
and numbers of errors were recorded.
Verbal fluency
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Controlled Oral Word Association Test
(COWAT; Delis, Kramer, Kaplan, & Ober, 2000;
Lezak et al., 2004). The COWAT assesses verbal
production as well as rule maintenance and
response monitoring. It was administered accord-
ing to standardized procedures using the target
letters F, A, and S. A total score for each partici-
pant was calculated, representing the total number
of words generated across all three trials after
deductions for rule violations, set-loss errors (i.e.,
words not beginning with target letters), and per-
severations (i.e., saying the same word more than
once).
Verbal attention and working memory
Digit Span (WAIS–III Digit Span; Wechsler,
1997). This test measures immediate recall of
auditory verbal information. Digit span forward
and digit span backward conditions were adminis-
tered according to WAIS–III standardized
procedures.
Verbal learning and memory
Rey Auditory Verbal Learning Test (RAVLT;
Lezak et al., 2004; Rey, 1964). This test measures
acquisition, storage, and retrieval of verbal infor-
mation. During the learning stage, participants
were read a list of 15 words five separate times
and were asked to recall as many words as they
were able after each presentation. Then, they were
read a new (interference trial) list of 15 words once
and were asked to recall those words. Participants
then were asked to freely recall as many words as
they could from the first list (immediate recall).
Following a 30-minute delay, participants were
again asked to recall as many words as they
could from the first list. The number of words
recalled and errors during the learning trials, inter-
ference trial, immediate recall, and delayed recall
NEUROCOGNITION IN MARIJUANA USERS 383
trials were recorded. The learning trials assessed
the participant’s immediate learning and tempor-
ary storage of verbal information. The interference
trial assessed immediate learning of new informa-
tion, presented only once. The immediate recall
trial assessed learning recall when the items were
not actively rehearsed in working memory. The
delayed recall trial performance represented learn-
ing that had been consolidated into memory.
Intrusion and perseverative errors were also tabu-
lated. Intrusion errors occurred when participants
responded with nonlist words. Perseverative errors
occurred when participants repeated responses dur-
ing a given trial.
Additional learning and memory variables were
calculated to best characterize performance. Loss
after consolidation was calculated as the percen-
tage of words recalled during delay relative to
words recalled during the final learning trial
(Takagi et al., 2011). Retroactive interference
(Trial 5 vs. immediate recall) and proactive inter-
ference (Trial 1 vs. interference) were examined. To
explore learning efficiency and strategy, bidirec-
tional serial ordering and response consistency
were calculated (Delis et al., 2000). Bidirectional
serial ordering refers to recall of stimulus words in
the same order as they are presented, forward or
backward. Response consistency measures how
often the same words are recalled from trial to
trial during free recall as a percentage of total
words recalled during free recall trials:
Conjoint recall of words between Trial 6; 7
 100
ðT6; T7Þ=2
Spatial memory
Spatial Span. This test measures immediate
recall of visually presented nonverbal information
and is a nonverbal analog of the Digit Span Test.
The version used here was computerized using E-
prime Version 1.1 (Psychology Software Tools;
www.psnet.com). Participants, seated at a compu-
ter terminal, viewed arrays of squares on the
screen. One by one, some of the squares “lit up”
in a sequence. In the forward condition, partici-
pants repeated the sequence by touching the
squares in the remembered sequence using a
touch-pen device (FastPoint Technologies, Inc.).
In the backward condition, participants repeated
the sequence in reverse order. The forward and
backward memory spans were recorded as the
number of items recalled in correct sequence across
trials in each condition.
 384 BECKER, COLLINS, LUCIANA
Spatial Recognition (Cambridge
Neuropsychological Test Automated Battery,
CANTAB; Fray, Robbins, & Sahakian,
1996). This test measures recognition memory
for spatial locations. The participant viewed
empty boxes at different locations on the screen.
Five stimuli were presented in succession at differ-
ent locations on the screen for 3 s each. After a 5-s
delay, the participant was shown two boxes, one of
which was in a location previously displayed in the
earlier sequence. The participant indicated which
box position was shown previously. Accuracy and
response time were recorded. The percentage of
correct trials across all four blocks was used as
the variable of interest.
Downloaded by [Universidad Nacional Colombia] at 12:24 09 February 2015
Self-Ordered Search (CANTAB; Owen, Downes,
Sahakian, Polkey, & Robbins, 1990). This test
measures spatial working memory, self-monitor-
ing, and behavioral self-organization. Using a
computerized touch-screen, participants searched
for blue tokens hidden inside an array of boxes.
The task was organized into 4-, 6-, and 8-box
problems, with increased box number correspond-
ing to increased task difficulty. Participants were
instructed that at any one time there would be a
single token hidden inside one of the boxes. Their
task was to search until they found it, at which
point the next token would be hidden. Once a
given box yielded a token, that box would not be
used to hide the token again during the trial. Every
box was used once on every trial; thus, the total
number of tokens to be found during each trial
corresponded to the number of boxes on the
screen. A “between-search” error was recorded
when participants returned to open a box in
which a token had already been found.
Additionally, a strategy score was tabulated. The
strategy score, which was based on responses to 6-
and 8-item searches, reflects the participant’s ten-
dency to search through available locations in an
organized fashion. Between-search error scores for
each level of search complexity, as well as strategy
scores, were the variables of interest.
Spatial Delayed Response Task (DRT; Luciana
& Collins, 1997; Luciana, Collins, & Depue,
1998). This task measures working memory for
the locations of spatial targets. During each of 48
trials, the participant first observed a central fixa-
tion point on a computer monitor. Next, a visual
cue appeared in their peripheral vision for 200 ms.
After the peripheral visual cue, the cue and fixation
point disappeared, and the screen blackened for
randomly interspersed delay intervals of 500 or
8000 ms. After the delay interval, the participant
indicated the remembered location of the cue with
a touch-pen device (FastPoint Technologies, Inc.).
A block of 16 “no delay” trials were also adminis-
tered prior to the delay trials to measure basic
perceptual and visuomotor abilities independent
of memory. Average accuracy (in millimeters)
and response times (in milliseconds) were recorded
for each condition.
Planning
Tower of London (CANTAB; Owen et al.,
1990). This test measures future planning ability.
A full task description can be found in Luciana
et al. (2009). Using a computerized touch-screen,
participants moved colored balls to match a target
display (problem-solving block). Participants were
told at the start of each problem-solving trial that
the trial should be completed in X number of
moves, where X was the minimum number of
moves required to achieve a perfect solution. The
total number of problems in which participants
responded with the minimum number of moves
was recorded and was expressed as a proportion
of total possible perfect solutions. Participants
were instructed not to make the first move until
they knew which balls to move and were encour-
aged to solve the problem correctly on the first try.
Time from presentation of the problem to starting
to solve the problem (planning time) was recorded.
Planning time and percentage of perfect solutions
were examined.
Motivated decision making
Iowa Gambling Task (IGT: Bechara, Damasio,
Damasio, & Anderson, 1994). This task measures
motivated decision-making ability. Participants com-
pleted a computerized version of the IGT (Hooper,
Luciana, Conklin, & Yarger, 2004) during which they
selected from among four decks of cards varying in
their amounts of monetary reward and punishment
(Bechara et al., 1994). Participants worked to earn
real money (maximum of $5). For each selection
from Decks 1 or 2 (the “disadvantageous decks”),
participants would win $0.25 but the losses were
organized so that over 20 selections from these
decks, participants would incur a net loss of $1.25.
The difference between Decks 1 and 2 was in the
frequency and magnitude of punishment: Deck 1 con-
tained frequent (50% of cards) punishments, whereas
Deck 2 contained less frequent (10% of cards) but
much larger punishments. For each selection from
Decks 3 or 4 (the “advantageous decks”), participants
would win either $0.10 or $0.15, and the losses were
organized so that over 20 selections from these decks,

participants would accrue a net gain of $1.25. Similar
to the disadvantageous decks, the two advantageous
decks differed from each other in the frequency of
punishment, such that small punishments occurred
on 50% of the cards in Deck 3, and larger punish-
ments occurred on 10% of the cards in Deck 4. Trials
(n = 100) were split into five blocks with 20 trials per
block. For each block, the number of choices from
disadvantageous decks was subtracted from number
of choices from advantageous decks. Thus, values
above “0” correspond to relatively advantageous
choices. In addition, the actual numbers of selections
made from each deck were tabulated across the full
task to analyze choice preferences.
Together, these measures took several hours to
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complete.
Self-report questionnaires
Participants completed Achenbach’s Adult Self-
Report (ASR; Achenbach & Rescorla, 2003) ques-
tionnaire, which yields assessments of internalizing
and externalizing tendencies as well as answers to
specific substance use questions. Substance use
scales consist of self-reported daily tobacco use,
number of days drunk, and days using drugs
(other than alcohol or tobacco) for the previous 6
months.
Marijuana users completed the Personal
Experience Inventory (Henley & Winters, 1989)
to assess other substance use. The PEI measures
the frequency of substance use within the last 3
months on a 5-point scale (never, 1–5 times, 6–20
times, 21–49 times, 50–99 times, 100+ times).
Nonmarijuana drug use was calculated by sum-
ming the frequency ratings across illicit drug
classes (psychedelics, cocaine, amphetamines, bar-
biturates, tranquilizers, heroin, narcotics, steroids,
inhalants, and recreation use of prescription
drugs). Controls had no history of use of these
other substances.
Statistical approach
Data were analyzed using the Statistical Package
for the Social Sciences (SPSS Inc., Chicago, IL,
USA), Windows Version 19. Distributions of all
variables were examined. Error variables for the
Letter Cancellation, RAVLT, and COWAT tasks
were square root transformed to meet assumptions
for parametric analysis. Chi-square tests were used
to compare nominal variables (i.e., sex) between
marijuana users and controls. Mann–Whitney U
analyses assessed for group differences in substance
use characteristics, in which variances were
NEUROCOGNITION IN MARIJUANA USERS 385
unequal between groups. Univariate and repeated
measures analyses of variance (ANOVAs) assessed
for group differences in other characteristics. Sex,
IQ, and alcohol use were covaried in all group
comparisons. To best characterize a wide variety
of alcohol use patterns, alcohol use was quantified
as an average of two alcohol use variables that
were standardized across the whole sample (con-
trols and marijuana users). The first alcohol use
variable was calculated by multiplying the partici-
pants’ self-reported average drinking occasions per
week and the average number of alcoholic drinks
per occasion for the previous 6 months, as assessed
by direct interview. The second alcohol use vari-
able was the number of days that the participant
reported being drunk in the last 6 months, as
assessed by the ASR questionnaire. Missing data
from 2 controls and 1 marijuana user on an alco-
hol use variable reduced the sample size to 35
participants per group.
Due to recruitment procedures, controls had no
history of tobacco use or non-alcohol-related drug
use. Non-alcohol-related drug use was calculated
from responses on the PEI. Tobacco use was quan-
tified by responses to questions from the ASR and
K-SADS regarding patterns of daily use.
Accordingly, levels of alcohol, tobacco, and
other drug use differed between groups, but alco-
hol use was the only variable that could be used in
between-group analyses. The contributions of
tobacco and other drug use to cognition in the
marijuana users were examined within marijuana
users using partial correlations to explore the
extent to which other substance use contributed
to domains where group differences were observed.
Alcohol use, tobacco use, and nonmarijuana drug
use were correlated with task performance in mar-
ijuana users, controlling for IQ, sex, and other
substance use. For example, the examination of
alcohol effects controlled for tobacco and other
non-marijuana-related drug use.
Scatterplots of residuals were examined to assess
for normal distributions, and data were screened
for outliers and influential data points. To provide
a conservative control for the number of statistical
comparisons, alpha levels equal to or below .01
were considered significant, and alpha levels at or
below .05 were considered trend effects.
RESULTS
Demographics
Groups were comparable in age, years of educa-
tion, race/ethnic distribution, and IQ. Consistent
 386 BECKER, COLLINS, LUCIANA

with similar studies of drug users with demogra- TABLE 2

phically matched college student controls (Croft, Lifetime other drug usage in marijuana users
Mackay, Mills, & Gruzelier, 2001), IQs were gen- 1–5 6–10 11–15 Mean of total
erally above average, indicating that participants Substance times times times times
were generally high functioning from a cognitive
Cannabis
standpoint. There were significantly more males
Hash 1 0.14 (0.85)
among marijuana users, consistent with the gender
Stimulants
distribution of marijuana users in this age range Adderall 4 1 0.70 (2.06)
(Substance Abuse and Mental Health Services Cocaine 2 1 0.33 (1.34)
Administration, 2013). (See Table 1.) Opioids
Vicodin 5 0.39 (1.35)
Codeine 1 0.06 (0.34)
Substance use characteristics Opium 4 0.26 (0.79)
Oxycodone 2 0.05 (0.24)
Marijuana users had significantly higher alcohol Psychedelics
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use as assessed by averaging the standardized Mushrooms/ 16 3 2 1.24 (2.39)

scores of typical alcohol use patterns and days LSD
drunk in the past 6 months (p < .001; Table 1). Salvia 4 0.31 (1.08)
Mescaline 1 0.03 (0.17)
Additionally, as would be expected from national
Benzodiazepines
norms (Substance Abuse and Mental Health
Xanax 3 1 0.09 (0.28)
Services Administration, 2013), marijuana users Valium 1 0.11 (0.69)
had greater tobacco use, days drunk, and days Sedative/
using other drugs in the last 6 months than did hypnotics
controls. As a result of exclusion criteria, controls Ambien 1 0.29 (1.69)
reported no marijuana use. Marijuana users Other
reported a mean age of initiation of marijuana Ecstasy 12 0.81 (1.48)
use during midadolescence (M = 15.24, SD = Nitrous oxide 2 0.17 (0.86)
1.24). Marijuana users reported nearly daily mar- Note. Number of participants who used each drug at differ-
ijuana use during the past 30 days with a mean of ent usage levels.
10.20 hits per day; however, there was considerable
variability in the number of reported hits per day,
with a standard deviation of 9.12.

TABLE 3
DSM–IV–TR diagnostic characteristics
DSM–IV–TR diagnostic characteristics of marijuana user
Despite differences from the control sample, mar- sample. Total number of marijuana users that met criteria
ijuana users reported relatively little substance use Current
outside of marijuana and alcohol. The majority of Diagnosis Current Past and past
marijuana users had tried other drugs fewer than 5
times, and no participant had used any other drug Marijuana dependence 18 18 17
Marijuana abuse 12 14 12
more than 15 times (Table 2). Almost all marijuana Alcohol dependence 0 0 0
users met criteria for current and/or past marijuana Alcohol abuse 11 16 10
substance use disorder (SUD; Table 3), and many Bipolar NOS 1 1 0
met criteria for current and past alcohol abuse.1 Oppositional defiant disorder 0 2 0
There was high concordance between current and Specific phobia 0 1 0
past diagnosis of an SUD within subjects (Table 3). Comorbidity
Only marijuana 14 9
SUD symptom patterns were examined in detail to
dependence
clarify symptom expression related to alcohol, mar- Only marijuana abuse 6 6
ijuana, and other drug use. Marijuana users exhib- Only alcohol abuse 2 0
ited fewer symptoms related to current alcohol use Marijuana dependence, 3 9
(M = 0.89 symptoms per person, SD = 1.05) than alcohol abuse
Marijuana abuse, 6 7
related to marijuana use (M = 4.03 symptoms per
alcohol abuse

Note. Marijuana users: N = 35. DSM–IV–TR = Diagnostic

1
Note that the inclusion criterion of limiting alcohol use and Statistical Manual of Mental Disorders–Fourth Edition,
frequency to 4–5 drinks per occasion less than twice weekly Text Revision (American Psychiatric Association, 2000); NOS
still allows for the possibility of alcohol abuse symptoms. = not otherwise specified.

person, SD = 1.90; U = 100.5, p < .001). Similarly,
marijuana users reported fewer symptoms related to
past alcohol use (M = 1.20 symptoms per person, SD
= 1.32) than related to past marijuana use (M = 4.23
symptoms per person, SD = 1.77; U = 114.0, p <
.001). No SUD symptoms related to other drug use
were reported among marijuana users or controls. As
a result of exclusion criteria, controls exhibited very
few symptoms related to current alcohol use (M =
0.11 symptoms per person, SD = 0.32) or past alco-
hol use (M = 0.03 symptoms per person, SD = 0.17)
and no symptoms related to other drug use.
Comorbid psychopathology
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Given selection procedures, controls were free of
psychopathology. Outside of SUDs, marijuana
users reported little psychopathology (Table 3).
One participant met criteria for current bipolar
not otherwise specified (NOS); another met criteria
for past bipolar NOS. Both were due to episodic
hypomania, consistent with the reported comor-
bidity between SUDs and bipolar disorder (Perlis
et al., 2004; Wilens et al., 2008). Other psycholo-
gical disorders included past oppositional defiant
disorder (n = 2) and past specific phobia (n = 1).
As will be described, data were analyzed with and
without inclusion of these individuals.
Overall, the sample of marijuana users is notable
for its good overall psychological health indepen-
dent of marijuana use and for high levels of pre-
morbid functioning (as indicated through
estimated verbal IQ scores).
Neurocognitive performance
See Table 4.
Motor function
Groups were equivalent in Finger Tapping and
Grooved Pegboard performance with no evidence
of laterality differences.
Processing speed
Marijuana users demonstrated faster Letter
Cancellation completion times. Omission and com-
mission errors were equivalent between groups.
Completion times were uncorrelated with overall
errors in both groups. Groups were equivalent in
Digit Symbol performance.
NEUROCOGNITION IN MARIJUANA USERS 387
Verbal fluency (COWAT)
Marijuana users displayed greater verbal fluency,
producing more correct responses. Set-loss errors
were only marginally greater among users.
Perseverative errors were equivalent between groups.
Verbal learning and memory
The groups were equivalent on Digit Span forward
and backward.
A repeated measures analysis of covariance
(ANCOVA) across RAVLT trials (T1–T5, interfer-
ence trial, immediate recall, and delayed recall)
revealed a group effect, F(1, 65) = 7.31, p = .009,
ηp2 = .10, and a Group × Trial interaction, F(1, 65) =
8.74, p = .004, ηp2 = .12 (Figure 1). Follow-up ana-
lyses revealed that marijuana users had a trend
toward poorer performance during List Learning
Trial 5, F(1, 65) = 3.90, p = .05, ηp2 = .06.
Marijuana users performed worse than controls on
the interference trial list. Following interference,
marijuana users demonstrated poorer immediate
recall and poorer 30-minute delayed recall.
Furthermore, there was a trend for marijuana users
to have greater loss after consolidation, F(1, 65) =
6.30, p = .02, ηp2 = .09 (marijuana user M = 78.04%,
SD = 17.16; control M = 90.90%, SD = 16.76)
Examining retroactive interference (Trial 5 vs.
immediate recall) and proactive interference (Trial
1 vs. interference) revealed no significant trial by
group interactions. No significant group differ-
ences were noted during learning or delayed recall
for bidirectional serial ordering or response consis-
tency during learning. Marijuana users demon-
strated less response consistency between short-
and long-term recall, F(1, 65) = 15.78, p < .001,
ηp2 = .20 (marijuana user M = 80.64%, SD =
14.55; controls M = 93.73%, SD = 6.58).
Errors during list learning and recall were
equivalent between groups.
Spatial working memory
No significant group differences were evident on for-
ward or backward Spatial Span, Spatial Recognition,
or Spatial Self-Ordered Search. On the DRT, groups
were equivalent in their accuracy and response
latency for the no delay condition, indicating that
basic sensorimotor functions recruited by the task
were similar between groups. Additionally groups
displayed equivalent accuracy during the 500-ms
delay condition. Marijuana users demonstrated a
trend toward decreased accuracy on the 8000-ms
delay condition. Marijuana users had significantly
 388 BECKER, COLLINS, LUCIANA

TABLE 4
Neuropsychological battery scores

Control Marijuana user

Cognitive measure M (SD) M (SD) F p ηp2

Finger Tapping Test

Dominant hand (taps) 42.16 (10.19) 46.93 (7.19) 3.01 .087 .04
Nondominant hand (taps) 42.02 (8.49) 44.76 (7.65) 1.29 .261 .02
Grooved Pegboard
Dominant hand time (s) 65.41 (8.14) 64.12 (8.31) 0.32 .575 .01
Nondominant hand time (s)a 72.97 (9.98) 71.13 (11.55) 0.32 .572 .01
Letter Cancellation
Time (s) 111.95 (16.60) 96.79 (18.08) 7.50* .008 .10
Total omissionsc 1.51 (0.71) 1.49 (0.76) 0.01 .927 .00
Total commissionsc 0.81 (0.27) 0.72 (0.12) 1.42 .237 .02
Digit Symbol
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Total correct 87.59 (15.12) 89.35 (13.21) 0.17 .680 .00

COWAT–Verbal Fluency
Total correct words generated 43.24 (8.50) 50.79 (10.98) 6.78* .011 .09
Total set-loss errorsc 0.82 (0.29) 1.11 (0.52) 4.67^ .034 .07
Total perseverative errorsc 1.03 (0.39) 0.95 (0.41) 0.35 .557 .01
Digit Span
Digits forward (no. recalled) 7.52 (0.86) 6.99 (1.03) 3.28 .075 .05
Digits backward (no. recalled) 5.76 (1.19) 5.24 (1.17) 1.95 .167 .03
RAVLT–Verbal Learning and Memory
Total words: Trials 1–5 55.05 (7.00) 51.29 (8.34) 2.70 .105 .04
Total intrusions: Trials 1–5a 1.02 (0.58) 1.30 (0.63) 2.26 .121 .04
Total perseverative errors: Trials 1–5a 1.96 (0.78) 1.81 (1.01) 0.26 .609 .00
Total words: Interference trial list 7.40 (1.95) 5.83 (1.86) 9.08* .004 .12
Total words: Immediate recall 12.24 (2.08) 10.56 (2.44) 6.65* .012 .09
Total words: Delayed recall 12.03 (2.13) 9.68 (2.91) 10.47* .002 .14
Spatial Span
Forward (no. recalled) 6.55 (0.98) 6.99 (0.89) 2.17 .145 .03
Backward (no. recalled) 6.78 (1.22) 6.50 (1.01) 0.66 .421 .01
Spatial Recognitiona
% Correct recall 86.50 (8.14) 85.66 (7.20) 0.12 .731 .00
Self-Ordered Searcha
Between search errors 4 0.12 (0.49) 0.18 (0.44) 0.15 .700 .00
Between search errors 6 2.79 (3.25) 2.60 (2.67) 0.04 .835 .00
Between search errors 8 10.65 (9.02) 9.66 (8.32) 0.13 .716 .00
Total between search errors 13.56 (10.21) 12.43 (9.70) 0.13 .720 .00
Strategy score: 6–8 30.28 (5.36) 28.80 (5.52) 0.76 .386 .01
Spatial Delayed Response Task
Error: No delay (mm) 2.44 (0.76) 2.55 (0.88) 0.17 .682 .00
Error: 500-ms delay (mm) 6.44 (2.18) 7.70 (2.23) 3.15 .080 .05
Error: 8000-ms delay (mm) 9.87 (3.36) 11.98 (2.55) 4.81^ .032 .07
Mean reaction time: No delay (ms) 1823.33 (575.62) 1962.42 (419.96) 0.75 .390 .01
Mean reaction time: 500-ms delay (ms) 1663.24 (352.62) 2034.85 (374.35) 10.93* .002 .14
Mean reaction time: 8000-ms delay (ms) 1733.73 (345.42) 2234.00 (475.77) 15.60* <.000 .19
Tower of Londona
% Perfect solutions 83.71 (13.33) 74.12 (14.47) 5.24^ .025 .08
Average moves 2 2.00 (0.00) 2.00 (0.00)
Average moves 3 3.00 (0.16) 3.28 (0.39) 8.63* .005 .12
Average moves 4 4.92 (0.89) 5.16 (0.97) 0.72 .398 .01
Average moves 5 5.65 (1.00) 6.24 (1.13) 3.11 .083 .05
First move initiation time 2 3190.52 (1161.58) 3662.26 (735.35) 2.27 .137 .05
First move initiation time 3 5510.37 (2510.15) 5442.88 (1485.40) 0.01 .920 .00
First move initiation time 4 8308.17 (5079.47) 8420.53 (3091.36) 0.01 .935 .00
First move initiation time 5 12,987.90 (6940.13) 8805.07 (5108.86) 4.75^ .033 .07
Average first move initiation time 7499.24 (3547.50) 6582.68 (2138.04) 0.94 .337 .01

(Continued )
 NEUROCOGNITION IN MARIJUANA USERS 389

TABLE 4
(Continued)

Control Marijuana user

Cognitive measure M (SD) M (SD) F p ηp2

Iowa Gambling Taskb

Good choices – bad choices: Block 1 –1.12 (9.58) –3.56 (7.18) 0.82 .368 .01
Good choices – bad choices: Block 2 3.25 (10.36) –2.13 (7.54) 3.85^ .054 .06
Good choices – bad choices: Block 3 3.73 (9.48) –1.68 (8.67) 3.47 .067 .05
Good choices – bad choices: Block 4 9.56 (9.32) –1.29 (10.09) 12.73* .001 .17
Good choices – bad choices: Block 5 9.80 (10.42) –0.15 (10.66) 9.89* .003 .13
Good choices: Total 60.45 (18.17) 49.77 (16.10) 4.01^ .049 .06

Notes. Means reported are marginal means, controlling for sex, IQ, and alcohol use. COWAT = Controlled Oral Word Association
Test; RAVLT = Rey Auditory Verbal Learning Test. aData unavailable for 1 marijuana user (n = 34). bData unavailable for 1 control
(n = 34). cSquare root transformed.
^p ≤ .05. *p ≤ .01.
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Figure 1. Rey Auditory Verbal Learning Test (RAVLT) learning curve. Average words recalled during learning Trials 1–5,
interference trial (trialB), immediate recall, and 30-minute delayed recall. ^p ≤ .05. *p ≤ .01.

longer response latencies (slower performance) after Motivated decision making

both 500-ms and 8000-ms delays. Accuracy and
response latencies were uncorrelated in marijuana
users and controls for the 500-ms and 8000-ms
delay conditions.
Planning
There was a trend for marijuana users to pro-
duce fewer perfect solutions on the Tower of
London task, indicating that they made more
moves than necessary to achieve accurate perfor-
mance. When individual difficulty levels were
examined, marijuana users made significantly
more moves to complete three-move problems;
a similar pattern nominally characterized other
levels of difficulty. Additionally, marijuana users
had marginally faster initiation times during five-
move problems.
On the Iowa Gambling Task, total good minus
bad choices over five blocks of the task were exam-
ined with block as the within-subjects factor and
group as the between-subjects factor (Figure 2). A
significant main effect of group, F(1, 64) = 10.97, p
= .002, ηp2 = .15, was observed, with marijuana
users displaying poorer performance.
There was a significant group difference in
choice of Deck 1 [F(1, 64) = 7.63, p = .007, ηp2 =
.11] and Deck 2 [F(1, 64) = 7.77, p = .007, ηp2 =
.11], and a marginal group difference in choice of
Deck 4 [F(1, 64) = 5.26, p = .025, ηp2 = .08].
Marijuana users made more choices from disad-
vantageous decks, Decks 1 and 2, and fewer
choices from advantageous Deck 4 (Figure 3).
Deck choices were compared to choices expected
by chance. Both groups showed aversion to frequent
punishment decks (1 and 3), choosing from these less
 390 BECKER, COLLINS, LUCIANA
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Figure 2. Iowa Gambling Task. Total good choices minus total bad choices over five blocks. ^p ≤ .05. *p ≤ .01.

Figure 3. Iowa Gambling Task. Number of choices from each deck across five blocks between groups. ^p ≤ .05. *p ≤ .01.

often than expected at a significant or trend level:
Deck 1: marijuana user t(34) = –2.12, p = .041,
control t(33) = –7.43, p < .001; Deck 3: marijuana
user t(34) = –3.70, p = .001, control t(33) = –2.26, p =
.031. Within infrequent punishment decks, controls
demonstrated a preference for smaller wins with
infrequent smaller punishment [Deck 4: t(33) =
4.24, p < .001], with choices from Deck 4 correlating
with overall good choices throughout the task
(rsex, alcohol use, IQ = .80, p < .001). Conversely, mar-
ijuana users showed a preference for greater wins
with infrequent but greater punishment [Deck 2:
t(34) = 2.68, p = .011].
Associations with other substance use
For all significant group effects described above,
alcohol, tobacco, and nonmarijuana drug use were
each separately examined for associations with
task performance within marijuana users (Table 5).
 NEUROCOGNITION IN MARIJUANA USERS 391

TABLE 5 of London (TOL), greater alcohol use was unex-

Follow-up partial correlations between substance use variable pectedly associated with better task performance.
and cognitive measures in marijuana users controlling for sex
Alcohol use was not significantly correlated,
and IQ
using our stringent alpha level, with other task
Alcohol Tobacco Nonmarijuana performance variables.
Cognitive measure usea useb drug usec Furthermore, within marijuana users, no group
Letter Cancellation differences in cognitive function were noted between
time .10 –.20 .32 subjects with current alcohol abuse (n = 11) and
COWAT–Verbal subjects without current alcohol abuse (n = 24).
Fluency
Total words –.12 –.16 .03
Total set-loss errorsd –.21 –.04 –.32 Tobacco use
RAVLT–Verbal Cognitive performance was uncorrelated with
Learning & Memory
tobacco use within marijuana users (Table 5).
Total words: Trial 5 .47* –.15 .01
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Total words: .50* .11 .06

Interference trial list
Nonmarijuana drug use
Total words: .56* –.23 <–.01
Immediate recall There was a trend for nonmarijuana drug use to
Total words: Delayed .48* –.18 .33
be positively correlated with RAVLT delayed
recall
% of learning recalled .26 –.18 .43^ recall as well as with faster initiation times
during delay (decreased planning) on five-move Tower of
Delayed consistency .48* .07 .01 London problems.
Spatial Delayed
Response Task
Error: 8000-ms delay –.40^ .05 .14 Impact of comorbid psychopathology
Reaction time: 500 ms- –.28 –.29 .01
delay Significant group differences remained unchanged
Reaction time: 8000- –.30 –.21 <–.01 when marijuana users with psychopathology out-
ms delay
side of SUDs (n = 5) were excluded.
Tower of Londone
% Perfect solutions .35 .04 .05
Average moves 3 –.40^ –.24 –.20 DISCUSSION
First move initiation –.20 –.17 –.36^
time 5
This study employed a comprehensive neurocogni-
Iowa Gambling Task
Good choices – bad < –.01 –.13 –.15
tive battery to assess a range of cognitive abilities
choices: Block 2 in a low-risk sample of college-aged daily mari-
Good choices – bad .21 .09 –.08 juana users who were studied in a nonintoxicated
choices: Block 4 state but in the context of active use. The mari-
Good choices – bad –.04 .15 –.18 juana user sample was notable in terms of its rela-
choices: Block 5
Good choices: Total –.21 –.22 .14
tive psychological health, absence of externalizing
Deck 1 choices .05 –.08 <.01 psychopathology, and above-average levels of gen-
Deck 2 choices –.20 –.04 .24 eral intellect. Despite this general pattern of low
Deck 4 choices –.06 .09 –.22 risk, and in the context of several cognitive
Notes. COWAT = Controlled Oral Word Association Test; strengths, marijuana users demonstrated a number
RAVLT = Rey Auditory Verbal Learning Test. aControlling of cognitive deficits relative to demographically
for tobacco and nonmarijuana drug use. bControlling for alco- matched controls.
hol and nonmarijuana drug use. cControlling for alcohol and Marijuana users performed particularly well on
tobacco use. dSquare root transformed. eData unavailable for 1
speeded measures, such as letter cancellation and
participant (n = 34).
^p ≤ .05. *p ≤ .01. verbal fluency. Both measures are short tasks (<2
min), requiring short-term sustained attention. It is
important to note that these tasks are externally
motivated, with instructions to work quickly.
Alcohol use
On the other hand, marijuana users demon-
For learning and recall measures of the strated many relative deficits in the domains of
RAVLT, errors made within the 8000-ms delay memory, problem solving, and motivated decision
condition of the delayed response task, and aver- making. It appears marijuana users were generally
age moves on three-move problems of the Tower less motivated and, as a consequence, less
 392 BECKER, COLLINS, LUCIANA
persistent in the absence of motivation-enhancing
instruction, when tasks required sustained and
internally motivated effort. For instance, mari-
juana users’ verbal learning performance was char-
acterized by a pattern of sustained accurate
performance during early learning trials and a
slow and subtle divergence from controls’ perfor-
mance as the task progressed (see Figure 1).
Marijuana users demonstrated greater loss after
consolidation when required to produce learned
information after a time delay. Marijuana users’
relatively decreased response consistency indicates
use of a less efficient recall strategy. The observa-
tion of relatively poor retention of learned material
over time is consistent with other reports (Block
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et al., 2002; Fried et al., 2005; Medina et al., 2007;
Pope & Yurgelun-Todd, 1996; Tait, Mackinnon, &
Christensen, 2011; Takagi et al., 2011; Wagner et.
al., 2010) and could be explained by a combination
of deficits in executive control as well as motiva-
tion. While the loss of information may appear to
be relatively low in absolute magnitude (1 in 15
presented words), this same degree of information
loss in the context of ongoing academic, occupa-
tional, and social interactions could have obvious
impacts on social function and other areas of
achievement. Similarly, the Tower of London and
Iowa Gambling Tasks require sustained effort for
optimal performance, and the longer trials of the
delayed response task require intrinsically focused
attention during the delay interval to support accu-
rate responding (Luciana et al., 1998).
When these findings are considered in relation to
the areas where marijuana users demonstrated
relative strengths (short-term externally motivated
tasks that required quick performance), it could be
that marijuana users are most impaired when tasks
require intrinsic motivation and most successful
when tasks are enhanced by the provision of moti-
vation-enhancing instructions, such as the instruc-
tion to work quickly. External or extrinsic
motivation reflects motivation that is cued through
external means and is performance or incentive
based. In contrast, internal/intrinsic motivation is
reflected by a sense of purpose as well as voluntary
engagement with a task in the absence of obvious
external incentives (Lee, Reeve, Xue, & Xiong,
2012; Murayama, Matsumoto, Izuma, &
Matsumoto, 2010). The speeded tasks within our
battery can be construed as performance-based
measures of external motivation. To some extent,
all tasks in the battery require intrinsic motivation,
but voluntary engagement is most strongly
recruited when tasks are lengthy and require
increasing amounts of self-organization and focus
to assure accurate performance.
It has been proposed that a source of intrinsic
motivation is the subjective value of achieving suc-
cess on a task (Murayama et al., 2010). Subjective
value is modulated within the brain through the
dopaminergic reward network, including midbrain
structures, ventral and dorsal striatum, and the
prefrontal cortex (Kable & Glimcher, 2007; Levy
& Glimcher, 2011). These regions are involved in
both incentive (performance)-based and intrinsic
motivational tasks. The lateral prefrontal cortex
has been suggested as a substrate for the intrinsic
preparatory cognitive control necessary to pursue
distinct goals. In addition, conscious effort-based
processing has been associated with the anterior
cingulate and dorsolateral prefrontal cortices
(Mulert, Menzinger, Leicht, Pogarell, & Hegerl,
2005). A recent series of studies has further linked
personal agency and other aspects of intrinsic
motivation to activation in the anterior insular
region (Lee & Reeve, 2013; Lee et al., 2012).
Although most neuroscientific studies of motiva-
tion involve manipulations of external incentive-
based motivation, and studies of intrinsic motiva-
tion are limited, we propose that overlapping sub-
cortical systems are involved in both types of
motivation given that incentive-based learning
necessarily impacts subjective valuation but that
higher order frontal systems (involving multiple
regions of the prefrontal cortex) are more strongly
recruited in support of intrinsic motivation—the
pursuit of goals in the absence of obvious external
incentives.
These frontal systems are known to mediate
tasks in our battery where marijuana users demon-
strated deficits. For instance, success on delayed
recall trials of the RAVLT has been linked to
frontal mechanisms (Gershberg & Shimamura,
1995; N. M. Long, Oztekin, & Badre, 2010), and
multiple regions of the dorsal, medial, and ventral
prefrontal cortex, as well as the insular region,
contribute to successful IGT performance
(Bechara et al., 1994; Lawrence, Jollant, O’Daly,
Zelaya, & Phillips, 2009). Accordingly, we
hypothesize that neuroscience-based studies of
intrinsic versus extrinsic motivation in marijuana
users would reveal stronger evidence of disruption
in the former. Although this suggestion is specula-
tive, given that motivation was not directly mea-
sured in this study, motivation-enhancing
instruction has been found to improve marijuana
users’ performance, but not that of controls, on a
verbal learning and memory task (Macher &
Earleywine, 2012).
Several tasks in our battery, including the spatial
delayed response task, are heavily influenced by
dopamine neurotransmission in frontostriatal

circuits, with increased dopamine activity facilitat-
ing better performance (Luciana et al., 1998).
Similarly, acute but indirect reduction of dopami-
nergic activity has been found to produce impaired
decision-making performance on the Iowa
Gambling Task (Sevy et al., 2006), mirroring the
disruptions noted in the current study. Throughout
the Iowa Gambling Task, marijuana users failed to
acquire an effective strategy. Marijuana users’
choice patterns suggest that reward feedback was
more compelling to marijuana users than was pun-
ishment feedback.
The observed performance deficits on the IGT
and spatial delayed response task may indicate
blunted striatal or frontal dopamine activity in
Downloaded by [Universidad Nacional Colombia] at 12:24 09 February 2015
the marijuana users, a finding previously reported
in adult marijuana users (Kowal, Colzato, &
Hommel, 2011) and consistent with the animal
literature (Pistis et al., 2004; Schneider & Koch,
2003). A recent study examined dopamine synth-
esis capacity in regular marijuana users who
experienced psychotic-like symptoms while intoxi-
cated with nonusing sex- and age-matched control
subjects. Findings revealed diminished dopamine
synthesis capacity in marijuana users in multiple
regions of the striatum (Bloomfield et al., 2013).
Consistent with our proposed model, this dimin-
ished synthesis capacity was associated with a
younger age onset of marijuana use as well as
with higher current levels of use. A younger age
of marijuana use onset is also associated with dis-
rupted patterns of dopamine receptor binding
(Urban et al., 2012). Bloomfield et al. (2013) have
suggested that diminished striatal dopamine synth-
esis capacity accounts for amotivation in heavy
marijuana users. Further research directly asses-
sing dopaminergic activity in marijuana users and
its relation to cognitive performance is needed to
more comprehensively link dopamine activity to
behavior in this population.
The performance deficits observed in the cur-
rent study cohere with findings from the brain
imaging literature indicating less efficient brain
activation patterns in marijuana users.
Marijuana users demonstrate increased activation
across a wide range of brain regions and recruit
alternative brain networks during task perfor-
mance (Block et al., 2002; Chang, Yakupov,
Cloak, & Ernst, 2006; Harding et al., 2012;
Jacobsen, Mencl, Westerveld, & Pugh, 2004;
Kanayama, Rogowska, Pope, Gruber, &
Yurgelun-Todd, 2004; Padula, Schweinsburg, &
Tapert, 2007; Schweinsburg et al., 2010; Tapert
et al., 2007). Increased activation and recruitment
of alternative pathways may be compensatory
and less efficient.
NEUROCOGNITION IN MARIJUANA USERS 393
While marijuana users exhibited greater alcohol,
tobacco, and nonmarijuana drug use than controls,
it does not appear that most observed cognitive
differences were due to the impacts of these other
substances. For the majority of tasks, alcohol,
tobacco, and other substance use was unrelated to
task performance. However, within the domain of
verbal learning (RAVLT), relatively higher levels
of self-reported alcohol use in marijuana users
were associated with better cognitive functioning.
This pattern is consistent with recent reports of
more normative patterns of structural brain integ-
rity in marijuana users who use alcohol versus
those who do not (Jacobus et al., 2009; Medina
et al., 2007). While counterintuitive, this finding
may point to specific neural interactions between
alcohol and marijuana such that alcohol use bene-
fits some areas of memory consolidation function
in the context of heavy marijuana use.
Importantly, however, the interaction between
alcohol and marijuana, if present, does not protect
against diminished cognitive performance in other
areas of function when marijuana users are com-
pared to controls, nor does it ameliorate the overall
performance deficit noted between marijuana users
and controls on the RAVLT.
Moreover, when the limited number of users
with histories of non-substance-related psycho-
pathology were excluded, significant group differ-
ences remained. Marijuana users with and without
current alcohol abuse did not differ in cognitive
performance. Whether these findings would gener-
alize to marijuana users who exhibit high levels of
externalizing psychopathology or other forms of
economic or psychological risk is unknown, but
we speculate, based on the extant literature, that
the presence of additional risk factors would result
in an even more extensive pattern of group differ-
ences given that such factors are independently
associated with cognitive difficulties.
In summary, marijuana users demonstrated an
inconsistent pattern in terms of leveraging appro-
priate strategies to facilitate performance on com-
plex memory, planning, and decision-making
tasks. These tasks generally required high levels
of self-organization, as well as potentially greater
demands on intrinsic motivation, as opposed to
areas where the marijuana users excelled (fast,
short-term processing tasks), which were more
externally motivated. These findings suggest that
if individuals engage in use on a daily basis, they
may become increasingly dependent upon external
sources of reinforcement and motivation to struc-
ture their behavior as opposed to intrinsically dri-
ven self-reliance and self-organization. On the
other hand, they may excel in settings where
 394 BECKER, COLLINS, LUCIANA
external sources of motivation are high. Marijuana
users’ performance across domains of function sug-
gests the possibility of diminished frontostriatal
dopaminergic activity, affecting both decision-
making and spatial working memory performance.
This may be the mechanism driving the perfor-
mance deficits noted and may be one avenue
through which chronic marijuana use, particularly
use that is initiated during adolescence, impacts
longer term function.
Limitations
One limitation of the current study is the overrepre-
Downloaded by [Universidad Nacional Colombia] at 12:24 09 February 2015
sentation of males in the marijuana user sample.
However, this gender distribution is consistent with
the gender distribution of marijuana users in the
United States (Substance Abuse and Mental Health
Services Administration, 2013). Sex was controlled in
all statistical analyses; however, findings cannot be
readily generalized to female marijuana users. A
further limitation is that our design does not permit
dose–response associations to be measured in mari-
juana users who tended to be relatively homogeneous
in their use patterns. A related issue is that it is difficult
to quantify the precise amount of drug ingested by
marijuana users given that the potency of marijuana is
not standard. While many studies have quantified
dose by calculating hits per day (which we assessed),
this measure does not address potency or the amount
of drug ingested during a hit. Marijuana users were
required to use marijuana at least 5 days per week,
yielding a relatively homogeneous sample of mari-
juana users. There were no requirements for amount
of hits during each episode of use.
Additionally, while marijuana users were not
acutely high during testing, we cannot rule out the
possibility that the cognitive differences observed in
our sample are due to residual effects of marijuana
use. However, the current assessment provides a
comprehensive cognitive profile of otherwise high-
functioning individuals in the context of frequent
current marijuana use. This profile allows us to
make real-world inferences about how daily mari-
juana use might impact cognition. In order to mini-
mize potential confounds, we recruited high-
functioning individuals, with comparable education
and IQ to those of other college-aged controls, and a
low level of psychopathology. While this feature of
the study can be considered a strength, since the
sample of users represents college-aged individuals
who heavily use the drug, it may limit generalizabil-
ity to other marijuana-using samples who evidence
more externalizing behavior, less education, and
more psychopathology. Our expectation is that they
would show greater levels of impairment.
Another possible concern is that marijuana users
were in active states of withdrawal during testing,
affecting the results. Marijuana users were asked to
abstain for at least a 12-hour period prior to the
study. This possibility appears unlikely given the
psychomotor performance exhibited by marijuana
users, which is inconsistent with behaviors that
individuals in the midst of marijuana withdrawal
demonstrate (Haney et al., 2001). Finally, we did
not employ marijuana drug testing, since the active
compound in marijuana remains detectible long
after prior use. The level of detail that participants
conveyed regarding their use patterns was convin-
cing in terms of the likelihood that they were,
indeed, heavy marijuana users, an assumption vali-
dated by their reports of symptoms of marijuana
dependence. However, because we did not employ
drug testing, we cannot completely rule out the
possibility that actual use in these participants is
lower than what they self-reported. Finally,
although our findings are suggestive of patterns
of impairment that emerge as a consequence of
use and replicate findings reported in the literature,
cause–effect associations cannot be determined. It
could be that premorbid levels of function were
impaired in marijuana users prior to use onset.
We have suggested that marijuana use during
active stages of brain development is more likely to
result in cognitive impairment as opposed to use that
begins later in life. Our sample of marijuana users
had a relatively young age of marijuana use onset
(15.2 years) relative to national norms (Substance
Abuse and Mental Health Services Administration,
2013) with age of onset of use ranging from 13 to 18
years. This is an active period of brain and associated
cognitive development (Giedd et al., 1999; Lebel &
Beaulieu, 2011; Luciana, Conklin, Hooper, &
Yarger, 2005; Sowell, Thompson, Tessner, & Toga,
2001). The animal literature supports our hypothesis
that introducing marijuana during that critical time
could lead to long-standing cognitive effects, which
can be observed during assessment in adulthood,
while use is ongoing. An obvious area of continued
empirical study concerns the cognitive impacts of
marijuana use at varying ages of onset, which we
cannot comprehensively address within the current
dataset given small sample size. Independent of
length of drug exposure as a factor that might impact
the current findings, this study is nonetheless infor-
mative regarding the cognitive profiles of young
adults who are active marijuana users during the
college years. We speculate that such use will become
increasingly prevalent with marijuana legalization.

CONCLUSIONS
The current study provides a comprehensive cog-
nitive profile of college-aged daily marijuana users.
Marijuana users demonstrated strengths relative to
controls in processing speed and verbal fluency.
Marijuana users also demonstrated numerous cog-
nitive deficits, most notably in verbal memory,
engagement, and use of efficient strategies with
complex tasks, and motivated decision making.
Future dose–response studies in samples that are
similarly free of comorbid pathology and in this
well-defined age range would be helpful in clarify-
ing whether a single underlying deficit leads to
these distinct behavioral patterns.
Downloaded by [Universidad Nacional Colombia] at 12:24 09 February 2015
Pharmacological challenge or positron emission
tomography (PET) studies in marijuana users ver-
sus controls can further clarify the role that dopa-
mine activity plays in the observed behavioral
patterns. Additionally, the relationship between
concurrent marijuana and alcohol use and cogni-
tive performance should continue to be explored in
early-onset marijuana users to determine the
unique and combined effects of the substances on
performance.
REFERENCES
Achenbach, T. M., & Rescorla, L. A. (2003). Manual for
the ASEBA Adult Forms & Profiles. Burlington, VT:
University of Vermont, Research Center for
Children, Youth, & Families.
American Psychiatric Association. (2000). Diagnostic
and statistical manual of mental disorders (4th ed.,
text rev.). Washington, DC: Author.
Bambico, F. R., Nguyen, N. T., Katz, N., & Gobbi, G.
(2010). Chronic exposure to cannabinoids during
adolescence but not during adulthood impairs emo-
tional behaviour and monoaminergic neurotransmis-
sion. Neurobiology of Disease, 37(3), 641–655.
Bartholomew, J., Holroyd, S., & Heffernan, T. M.
(2010). Does cannabis use affect prospective memory
in young adults? Journal of Psychopharmacology, 24
(2), 241–246. doi:10.1177/0269881109106909
Battisti, R. A., Roodenrys, S., Johnstone, S. J., Pesa, N.,
Hermens, D. F., & Solowij, N. (2010). Chronic can-
nabis users show altered neurophysiological function-
ing on Stroop task conflict resolution.
Psychopharmacology (Berl), 212(4), 613–624.
doi:10.1007/s00213-010-1988-3
Bechara, A., Damasio, A. R., Damasio, H., &
Anderson, S. W. (1994). Insensitivity to future con-
sequences following damage to human prefrontal cor-
tex. Cognition, 50(1–3), 7–15.
Block, R. I., O’Leary, D. S., Hichwa, R. D.,
Augustinack, J. C., Boles Ponto, L. L., Ghoneim,
M. M., … Andreasen, N. C. (2002). Effects of fre-
quent marijuana use on memory-related regional cer-
ebral blood flow. Pharmacology, Biochemistry, and
Behavior, 72, 237–250.
NEUROCOGNITION IN MARIJUANA USERS 395
Bloomfield, M. A. P., Morgan, C. J. A., Egerton, A.,
Kapur, S., Curran, H. V., & Howes, O. D. (2013).
Dopaminergic function in cannabis users and its rela-
tionship to cannabis-induced psychotic symptoms.
Biological Psychiatry. Advance online publication.
doi:10.1016/j.biopsych.2013.05.027
Bolla, K. I., Brown, K., Eldreth, D., Tate, K., & Cadet,
J. L. (2002). Dose-related neurocognitive effects of
marijuana use. Neurology, 59(9), 1337–1343.
Chang, L., Yakupov, R., Cloak, C., & Ernst, T. (2006).
Marijuana use is associated with a reorganized visual-
attention network and cerebellar hypoactivation.
Brain, 129, 1096–112. doi:10.1093/brain/awl064
Clark, L., Roiser, J. P., Robbins, T. W., & Sahakian, B.
J. (2009). Disrupted “reflection” impulsivity in can-
nabis users but not current or former ecstasy users.
Journal of Psychopharmacology, 23, 14–22.
doi:10.1177/0269881108089587
Crean, R. D., Crane, N. A., & Mason, B. J. (2011). An
evidence-based review of acute and long-term effects
of cannabis use on executive cognitive functions.
Journal of Addiction Medicine, 5(1), 1–8.
Croft, R. J., Mackay, A. J., Mills, A. T. D., & Gruzelier,
J. G. H. (2001). The relative contributions of ecstasy
and cannabis to cognitive impairment.
Psychopharmacology (Berl), 153(3), 373–379.
Cuttler, C., McLaughlin, R. J., & Graf, P. (2012).
Mechanisms underlying the link between cannabis
use and prospective memory. PloS One, 7(5),
e36820. doi:10.1371/journal.pone.0036820
Delis, D. C., Kramer, J. H., Kaplan, E., & Ober, B. A.
(2000). California Verbal Learning Test–Second
Edition. San Antonio, TX: Psychological
Corporation.
Dougherty, D. M., Mathias, C. W., Dawes, M. A., Furr,
R. M., Charles, N. E., Liguori, A., … Acheson, A.
(2013). Impulsivity, attention, memory, and decision-
making among adolescent marijuana users.
Psychopharmacology (Berl), 226, 307–319.
doi:10.1007/s00213-012-2908-5
Ehrenreich, H., Rinn, T., Kunert, H. J., Moeller, M. R.,
Poser, W., Schilling, L., … Hoehe, M. R. (1999).
Specific attentional dysfunction in adults following
early start of cannabis use. Psychopharmacology
(Berl), 142(3), 295–301.
Ellgren, M., Artmann, A., Tkalych, O., Gupta, A.,
Hansen, H. S., Hansen, S. H., … Hurd, Y. L.
(2008). Dynamic changes of the endogenous canna-
binoid and opioid mesocorticolimbic systems during
adolescence: THC effects. European
Neuropsychopharmacology, 18(11), 826–834.
doi:10.1016/j.euroneuro.2008.06.009
Fontes, M. A., Bolla, K. I., Cunha, P. J., Almeida, P. P.,
Jungerman, F., Laranjeira, R. R., … Lacerda, A. L. T.
(2011). Cannabis use before age 15 and subsequent execu-
tive functioning. The British Journal of Psychiatry, 198
(6), 442–447. doi:10.1192/bjp.bp.110.077479
Fray, P. J., Robbins, T. W., & Sahakian, B. J. (1996).
Neuropsychiatric applications of CANTAB.
International Journal of Geriatric Psychiatry, 11,
329–336.
Freund, T. F., Katona, I., & Piomelli, D. (2003). Role of
endogenous cannabinoids in synaptic signaling.
Physiological Review, 83, 1017–1066.
Fried, P. A., Watkinson, B., & Gray, R. (2005).
Neurocognitive consequences of marihuana—A com-
parison with pre-drug performance. Neurotoxicology
 396 BECKER, COLLINS, LUCIANA
and Teratology, 27(2), 231–239. doi:10.1016/j.
ntt.2004.11.003
Gershberg, F. B., & Shimamura, A. P. (1995). Impaired
use of organizational strategies in free recall following
frontal lobe damage. Neuropsychologia, 13(10), 1305–
1333.
Giedd, J. N., Blumenthal, J., Jeffries, N. O., Castellanos,
F. X., Liu, H., Zijdenbos, A., … Rapoport, J. L.
(1999). Brain development during childhood and ado-
lescence: A longitudinal MRI study. Nature
Neuroscience, 2(10), 861–863. doi:10.1038/13158
Gogtay, N., & Thompson, P. M. (2010). Mapping gray
matter development: Implications for typical devel-
opment and vulnerability to psychopathology. Brain
and Cognition, 72, 6–15. doi:10.1016/j.
bandc.2009.08.009
Gonzalez, R., Schuster, R. M., Mermelstein, R. J.,
Vassileva, J., Martin, E. M., & Diviak, K. R.
Downloaded by [Universidad Nacional Colombia] at 12:24 09 February 2015
(2012). Performance of young adult cannabis users
on neurocognitive measures of impulsive behavior
and their relationship to symptoms of cannabis use
disorders. Journal of Clinical and Experimental
Neuropsychology, 34(9), 962–976. doi:10.1080/
13803395.2012.703642
Grant, J. E., Chamberlain, S. R., Schreiber, L., &
Odlaug, B. L. (2012). Neuropsychological deficits
associated with cannabis use in young adults. Drug
and Alcohol Dependence, 121, 159–162. doi:10.1016/j.
drugalcdep.2011.08.015
Gruber, S. A., Sagar, K. A., Dahlgren, M. K., Racine,
M., & Lukas, S. E. (2012). Age of onset of marijuana
use and executive function. Psychology of Addictive
Behaviors, 26(3), 496–506. doi:10.1037/a0026269
Haney, M., Ward, A. S., Comer, S. D., Hart, C. L.,
Foltin, R. W., & Fischman, M. W. (2001). Bupropion
SR worsens mood during marijuana withdrawal in
humans. Psychopharmacology, 155(2), 171–179.
doi:10.1007/s002130000657
Hanson, K. L., Winward, J. L., Schweinsburg, A. D.,
Medina, K. L., Brown, S. A., & Tapert, S. F. (2010).
Longitudinal study of cognition among adolescent
marijuana users over three weeks of abstinence.
Addictive Behaviors, 35(11), 970–976. doi:10.1016/j.
addbeh.2010.06.012
Harding, I. H., Solowij, N., Harrison, B. J., Takagi, M.,
Lorenzetti, V., Lubman, D. I., … Yücel, M. (2012).
Functional connectivity in brain networks underlying
cognitive control in chronic cannabis users.
Neuropsychopharmacology, 37(8), 1923–1933.
doi:10.1038/npp.2012.39
Harvey, M. A., Sellman, J. D., Porter, R. J., &
Frampton, C. M. (2007). The relationship between
non-acute adolescent cannabis use and cognition.
Drug and Alcohol Review, 26(3), 309–319.
doi:10.1080/09595230701247772
Heng, L., Beverley, J. A., Steiner, H., & Tseng, K. Y.
(2011). Differential developmental trajectories for
CB1 cannabinoid receptor expression in limbic/asso-
ciative and sensorimotor cortical areas. Synapse, 65
(4), 278–286. doi:10.1002/syn.20844
Henley, G. A., & Winters, K. C. (1989). Development of
psychosocial scales for the assessment of adolescents
involved with alcohol and drugs. International
Journal of Addictions, 24, 973–1001.
Hooper, C. J., Luciana, M., Conklin, H. M., & Yarger, R. S.
(2004). Adolescents’ performance on the Iowa Gambling
Task: Implications for the development of decision mak-
ing and ventromedial prefrontal cortex. Developmental
Psychology, 40(6), 1148–1158. doi:10.1037/0012-
1649.40.6.1148
Jacobsen, L. K., Mencl, W. E., Westerveld, M., & Pugh, K.
R. (2004). Impact of cannabis use on brain function in
adolescents. Annals of the New York Academy of
Sciences, 1021, 384–390. doi:10.1196/annals.1308.053
Jacobus, J., McQueeny, T., Bava, S., Schweinsburg, B.
C., Frank, L. R., Yang, T. T., & Tapert, S. F. (2009).
White matter integrity in adolescents with histories of
marijuana use and binge drinking. Neurotoxicology
and Teratology, 31(6), 349–355. doi:10.1016/j.
ntt.2009.07.006
Jager, G., & Ramsey, N. F. (2008). Long-term conse-
quences of adolescent cannabis exposure on the
development of cognition, brain structure and func-
tion: An overview of animal and human research.
Current Drug Abuse Reviews, 1(2), 114–123.
Johnston, L. D., Bachman, J. G., & Schulenberg, J. E.
(2012). Monitoring the Future national survey results
on drug use, 1975–2011: Volume II. College students
and adults ages 19–50. Ann Arbor, MI: Institute for
Social Research, The University of Michigan.
Johnston, L. D., O’Malley, P. M., Bachman, J. G., &
Schulenberg, J. E. (2013). Monitoring the Future
national results on drug use: 2012 overview, key find-
ings on adolescent drug use. Ann Arbor, MI: Institute
for Social Research, The University of Michigan.
Kable, J. W., & Glimcher, P. W. (2007). The neural
correlates of subjective value during intertemporal
choice. Nature Neuroscience, 10(12), 1625–1633.
doi:10.1038/nn2007
Kanayama, G., Rogowska, J., Pope, H. G., Gruber, S.
A., & Yurgelun-Todd, D. A. (2004). Spatial working
memory in heavy cannabis users: A functional mag-
netic resonance imaging study. Psychopharmacology
(Berl), 176, 239–247. doi:10.1007/s00213-004-1885-8
Kaufman, J., Birmaher, B., Brent, D., Rao, U., Flynn,
C., Moreci, P., … Ryan, N. (1997). Schedule for
Affective Disorders and Schizophrenia for School-
Age Children–Present and Lifetime Version (K-
SADS-PL): Initial reliability and validity data.
Journal of the American Academy of Child and
Adolescent Psychiatry, 36(7), 980–988. doi:10.1097/
00004583-199707000-00021
Kowal, M. A., Colzato, L. S., & Hommel, B. (2011).
Decreased spontaneous eye blink rates in chronic
cannabis users: Evidence for striatal cannabinoid-
dopamine interactions. PloS One, 6(11), e26662.
doi:10.1371/journal.pone.0026662
Lafayette Instrument. (1989). Instruction manual for the
32025 Grooved Pegboard Test. Lafayette, IN: Author.
Lawrence, N. S., Jollant, F., O’Daly, O., Zelaya, F., &
Phillips, M. L. (2009). Distinct roles of prefrontal
cortical subregions in the Iowa Gambling Task.
Cerebral Cortex, 19(5), 1134–1143. doi:10.1093/cer-
cor/bhn154
Lebel, C., & Beaulieu, C. (2011). Longitudinal develop-
ment of human brain wiring continues from child-
hood into adulthood. The Journal of Neuroscience,
31(30), 10937–10947. doi:10.1523/JNEUROSCI.
5302-10.2011
Lee, W., & Reeve, J. (2013). Self-determined, but not
non-self-determined, motivation predicts activations
in the anterior insular cortex: An fMRI study of

personal agency. Social Cognitive and Affective
Neuroscience, 8(5), 538–545. doi:10.1093/scan/nss029
Lee, W., Reeve, J., Xue, Y., & Xiong, J. (2012). Neural
differences between intrinsic reasons for doing versus
extrinsic reasons for doing: An fMRI study.
Neuroscience Research, 73(1), 68–72. doi:10.1016/j.
neures.2012.02.010.Neural
Levy, D. J., & Glimcher, P. W. (2011). Comparing
apples and oranges: Using reward-specific and
reward-general subjective value representation in the
brain. The Journal of Neuroscience, 31(41), 14693–
14707. doi:10.1523/JNEUROSCI.2218-11.2011
Lezak, M. D., Howieson, D. B., & Loring, D. W. (2004).
Neuropsychological assessment (4th ed.). New York,
NY: Oxford University Press.
Lisdahl, K. M., Gilbart, E. R., Wright, N. E., &
Shollenbarger, S. (2013). Dare to delay? The impacts
of adolescent alcohol and marijuana use onset on
Downloaded by [Universidad Nacional Colombia] at 12:24 09 February 2015
cognition, brain structure, and function. Frontiers in
Psychiatry, 4, 53. doi:10.3389/fpsyt.2013.00053
Lisdahl, K. M., & Price, J. S. (2012). Increased mari-
juana use and gender predict poorer cognitive func-
tioning in adolescents and emerging adults. Journal of
the International Neuropsychological Society, 18(4),
678–688. doi:10.1017/S1355617712000276
Long, L. E., Lind, J., Webster, M., & Weickert, C. S. (2012).
Developmental trajectory of the endocannabinoid sys-
tem in human dorsolateral prefrontal cortex. BMC
Neuroscience, 13, 87. doi:10.1186/1471-2202-13-87
Long, N. M., Oztekin, I., & Badre, D. (2010). Separable
prefrontal cortex contributions to free recall. The
Journal of Neuroscience, 30(33), 10967–10976.
doi:10.1523/JNEUROSCI.2611-10.2010
Luciana, M., & Collins, P. F. (1997). Dopaminergic
modulation of working memory for spatial but not
object cues in normal humans. Journal of Cognitive
Neuroscience, 9(3), 330–347. doi:10.1162/
jocn.1997.9.3.330
Luciana, M., Collins, P. F., & Depue, R. A. (1998).
Opposing roles for dopamine and serotonin in the
modulation of human spatial working memory func-
tions. Cerebral Cortex, 8(3), 218–226.
Luciana, M., Collins, P. F., Olson, E. A., & Schissel, A.
M. (2009). Tower of London performance in healthy
adolescents: The development of planning skills and
associations with self-reported inattention and impul-
sivity. Developmental Neuropsychology, 34(4), 461–
475. doi:10.1080/87565640902964540
Luciana, M., Conklin, H. M., Hooper, C. J., & Yarger,
R. S. (2005). The development of nonverbal working
memory and executive control processes in adoles-
cents. Child Development, 76(3), 697–712.
doi:10.1111/j.1467-8624.2005.00872.x
Macher, R. B., & Earleywine, M. (2012). Enhancing
neuropsychological performance in chronic cannabis
users: The role of motivation. Journal of Clinical and
Experimental Neuropsychology, 34(4), 405–415.
doi:10.1080/13803395.2011.646957
McHale, S., & Hunt, N. (2008). Executive function def-
icits in short-term abstinent cannabis users. Human
Psychopharmacology, 23(5), 409–415. doi:10.1002/
hup.941
Medina, K. L., Hanson, K. L., Schweinsburg, A. D.,
Cohen-Zion, M., Nagel, B. J., & Tapert, S. F. (2007).
Neuropsychological functioning in adolescent mari-
juana users: Subtle deficits detectable after a month of
abstinence. Journal of the International
NEUROCOGNITION IN MARIJUANA USERS 397
Neuropsychological Society, 13(5), 807–820.
doi:10.1017/S1355617707071032
Montgomery, C., Seddon, A. L., Fisk, J. E., Murphy, P.
N., & Jansari, A. (2012). Cannabis-related deficits in
real-world memory. Human Psychopharmacology, 27,
217–225. doi:10.1002/hup.1273
Morrison, P. D., Zois, V., McKeown, D. A., Lee, T. D.,
Holt, D. W., Powell, J. F., … Murray, R. M. (2009).
The acute effects of synthetic intravenous delta9-tet-
rahydrocannabinol on psychosis, mood and cognitive
functioning. Psychological Medicine, 39(10), 1607–
1616. doi:10.1017/S0033291709005522
Mulert, C., Menzinger, E., Leicht, G., Pogarell, O., &
Hegerl, U. (2005). Evidence for a close relationship
between conscious effort and anterior cingulate cortex
activity. International Journal of Psychophysiology, 56
(1), 65–80. doi:10.1016/j.ijpsycho.2004.10.002
Murayama, K., Matsumoto, M., Izuma, K., & Matsumoto,
K. (2010). Neural basis of the undermining effect of
monetary reward on intrinsic motivation. Proceedings
of the National Academy of Sciences, 107(49), 20911–
20916. doi:10.1073/pnas.1013305107
Olson, E. A., Collins, P. F., Hooper, C. J., Muetzel, R.,
Lim, K. O., & Luciana, M. (2009). White matter
integrity predicts delay discounting behavior in 9- to
23-year-olds: A diffusion tensor imaging study.
Journal of Cognitive Neuroscience, 21(7), 1406–1421.
doi:10.1162/jocn.2009.21107
Owen, A. M., Downes, J. J., Sahakian, B. J., Polkey, C.
E., & Robbins, T. W. (1990). Planning and spatial
working memory following frontal lobe lesions in
man. Neuropsychologia, 28(10), 1021–1034.
Padula, C. B., Schweinsburg, A. D., & Tapert, S. F.
(2007). Spatial working memory performance and
fMRI activation interaction in abstinent adolescent
marijuana users. Psychology of Addictive Behaviors,
21(4), 478–487. doi:10.1037/0893-164X.21.4.478
Perlis, R. H., Miyahara, S., Marangell, L. B., Wisniewski,
S. R., Ostacher, M., DelBello, M. P., … Nierenberg, A.
A. (2004). Long-term implications of early onset in
bipolar disorder: Data from the first 1000 participants
in the Systematic Treatment Enhancement Program for
Bipolar Disorder (STEP-BD). Biological Psychiatry, 55
(9), 875–881. doi:10.1016/j.biopsych.2004.01.022
Pistis, M., Perra, S., Pillolla, G., Melis, M., Muntoni, A.
L., & Gessa, G. L. (2004). Adolescent exposure to
cannabinoids induces long-lasting changes in the
response to drugs of abuse of rat midbrain dopamine
neurons. Biological Psychiatry, 56, 86–94.
Pope, H. G., Gruber, A. J., Hudson, J. I., Cohane, G.,
Huestis, M. A., & Yurgelun-Todd, D. (2003). Early-
onset cannabis use and cognitive deficits: What is the
nature of the association? Drug and Alcohol
Dependence, 69(3), 303–310.
Pope, H. G., & Yurgelun-Todd, D. (1996). The residual
cognitive effects of heavy marijuana use in college
students. JAMA: The Journal of the American
Medical Association, 275(7), 521–527.
Ramaekers, J. G., Kauert, G., van Ruitenbeek, P.,
Theunissen, E. L., Schneider, E., & Moeller, M. R.
(2006). High-potency marijuana impairs executive
function and inhibitory motor control.
Neuropsychopharmacology, 31(10), 2296–2303.
doi:10.1038/sj.npp.1301068
Realini, N., Rubino, T., & Parolaro, D. (2009).
Neurobiological alterations at adult age triggered by
adolescent exposure to cannabinoids.
 398 BECKER, COLLINS, LUCIANA
Pharmacological Research, 60(2), 132–138.
doi:10.1016/j.phrs.2009.03.006
Rey, A. (1964). L’examen de Clinique en Psychologie
[Clinical tests in psychology]. Paris: Presses
Universitaire de France.
Rodriguez de Fonseca, F., Ramos, J. A., Bonnin A., &
Fernandez-Ruiz, J. J. (1993). Presence of cannabinoid
binding sites in the brain from early postnatal ages.
Neuroreport, 4(2), 135–138.
Rubino, T., Realini, N., Braida, D., Guidi, S., Capurro, V.,
Vigano, D., … Parolaro, D. (2009). Changes in hippo-
campal morphology and neuroplasticity induced by ado-
lescent THC treatment are associated with cognitive
impairment in adulthood. Hippocampus, 19(8), 763–
772. doi:10.1002/hipo.20554
Schneider, M., & Koch, M. (2003). Chronic pubertal,
but not adult chronic cannabinoid treatment impairs
sensorimotor gating, recognition memory, and the
Downloaded by [Universidad Nacional Colombia] at 12:24 09 February 2015
performance in a progressive ratio task in adult rats.
Neuropsychopharmacology, 28(10), 1760–1769.
doi:10.1038/sj.npp.1300225
Schneider, M., & Koch, M. (2007). The effect of chronic
peripubertal cannabinoid treatment on deficient
object recognition memory in rats after neonatal
mPFC lesion. European Neuropsychopharmacology,
17(3), 180–186. doi:10.1016/j.euroneuro.2006.03.009
Schwartz, R. H., Gruenewald, P. J., Klitzner, M., &
Fedio, P. (1989). Short-term memory impairment in
cannabis-dependent adolescents. American Journal of
Diseases of Children, 143(10), 1214–1219.
Schweinsburg, A. D., Schweinsburg, B. C., Medina, K. L.,
McQueeny, T., Brown, S. A., & Tapert, S. F. (2010). The
influence of recency of use on fMRI response during
spatial working memory in adolescent marijuana users.
Journal of Psychoactive Drugs, 42(3), 401–412.
Sevy, S., Hassoun, Y., Bechara, A., Yechiam, E.,
Napolitano, B., Burdick, K., … Malhotra, A.
(2006). Emotion-based decision-making in healthy
subjects: Short-term effects of reducing dopamine
levels. Psychopharmacology (Berl), 188(2), 228–235.
Solowij, N., Jones, K. A., Rozman, M. E., Davis, S. M.,
Ciarrochi, J., Heaven, P. C. L., … Yücel, M. (2011).
Verbal learning and memory in adolescent cannabis
users, alcohol users and non-users.
Psychopharmacology (Berl), 216(1), 131–144.
doi:10.1007/s00213-011-2203-x
Solowij, N., Jones, K. A., Rozman, M. E., Davis, S. M.,
Ciarrochi, J., Heaven, P. C. L., … Yücel, M. (2012).
Reflection impulsivity in adolescent cannabis users: A
comparison with alcohol-using and non-substance-
using adolescents. Psychopharmacology (Berl), 219
(2), 575–586. doi:10.1007/s00213-011-2486-y
Sowell, E. R., Thompson, P. M., Tessner, K. D., &
Toga, A. W. (2001). Mapping continued brain
growth and gray matter density reduction in dorsal
frontal cortex: Inverse relationships during
postadolescent brain maturation. The Journal of
Neuroscience, 21(22), 8819–8829.
Substance Abuse and Mental Health Services
Administration. (2013). Results from the 2012 National
Survey on Drug Use and Health: Summary of national
findings, NSDUH Series H-46, HHS Publication No.
(SMA) 13-4795 (pp. 1–84). Rockville, MD: Author.
Tait, R. J., Mackinnon, A., & Christensen, H. (2011).
Cannabis use and cognitive function: 8-year trajec-
tory in a young adult cohort. Addiction, 106(12),
2195–2203. doi:10.1111/j.1360-0443.2011.03574.x
Takagi, M., Yücel, M., Cotton, S. M., Baliz, Y., Tucker,
A., Elkins, K., & Lubman, D. I. (2011). Verbal mem-
ory, learning, and executive functioning among ado-
lescent inhalant and cannabis users. Journal of
Studies on Alcohol and Drugs, 72(1), 96–105.
Tapert, S. F., Schweinsburg, A. D., Drummond, S. P.
A., Paulus, M. P., Brown, S. A., Yang, T. T., &
Frank, L. R. (2007). Functional MRI of inhibitory
processing in abstinent adolescent marijuana users.
Psychopharmacology (Berl), 194(2), 173–183.
doi:10.1007/s00213-007-0823-y
Urban, N. B. L., Slifstein, M., Thompson, J. L., Xu, X.,
Girgis, R. R., Raheja, S., … Abi-Dargham, A.
(2012). Dopamine release in chronic cannabis users:
A [11c]raclopride positron emission tomography
study. Biological Psychiatry, 71(8), 677–683.
doi:10.1016/j.biopsych.2011.12.018
Viveros, M.-P., Llorente, R., Moreno, E., & Marco, E.
M. (2005). Behavioural and neuroendocrine effects of
cannabinoids in critical developmental periods.
Behavioural Pharmacology, 16, 353–362.
Wagner, D., Becker, B., Gouzoulis-Mayfrank, E., &
Daumann, J. (2010). Interactions between specific para-
meters of cannabis use and verbal memory. Progress in
Neuro-Psychopharmacology & Biological Psychiatry, 34
(6), 871–876. doi:10.1016/j.pnpbp.2010.04.004
Wechsler, D. (1997). Manual for the Wechsler Adult
Intelligence Scale–Third Revision. San Antonio, TX:
The Psychological Corporation.
Wechsler, D. (1999). Manual for the Weschler
Abbreviated Scale of Intelligence. San Antonio, TX:
The Psychological Corporation.
Whitlow, C. T., Liguori, A., Livengood, L. B., Hart, S.
L., Mussat-Whitlow, B. J., Lamborn, C. M., …
Porrino, L. J. (2004). Long-term heavy marijuana
users make costly decisions on a gambling task.
Drug and Alcohol Dependence, 76(1), 107–111.
doi:10.1016/j.drugalcdep.2004.04.009
Wilens, T. E., Biederman, J., Adamson, J. J., Henin, A.,
Sgambati, S., Gignac, M., … Monuteaux, M. C.
(2008). Further evidence of an association between
adolescent bipolar disorder with smoking and sub-
stance use disorders: A controlled study. Drug and
Alcohol Dependence, 95(3), 188–198. doi:10.1016/j.
drugalcdep.2007.12.016